Changes in Sleep Architecture following Motor Learning Depend on Initial Skill Level

Abstract

Previous research has linked both rapid eye movement (REM) sleep and Stage 2 sleep to procedural memory consolidation. The present study sought to clarify the relationship between sleep stages and procedural memory consolidation by examining the effect of initial skill level in this relationship in young adults. In-home sleep recordings were performed on participants before and after learning the pursuit rotor task. We divided the participants into low- and high-skill groups based on their initial performance of the pursuit rotor task. In high-skill participants, there was a significant increase in Stage 2 spindle density after learning, and there was a significant correlation between the spindle density that occurred after learning and pursuit rotor performance at retest 1 week later. In contrast, there was a significant correlation between changes in REM density and performance on the pursuit rotor task during retest 1 week later in low-skill participants, although the actual increase in REM density failed to reach significance in this group. The results of the present study suggest the presence of a double dissociation in the sleep-related processes that are involved in procedural memory consolidation in low- and high-skill individuals. These results indicate that the changes in sleep microarchitecture that take place after learning depend on the initial skill level of the individual and therefore provide validation for the model proposed by Smith et al. [Smith, C. T., Aubrey, J. B., & Peters, K. R. Different roles for REM and Stage 2 sleep in motor learning. Psychologica Belgica, 44, 79-102, 2004]. Accordingly, skill level is an important variable that needs to be considered in future research on sleep and memory consolidation.

Sleep and time course of consolidation of visual discrimination skills in patients with narcolepsy–cataplexy

“…However, the potential indications of the lower effectiveness of sleep of NC patients were not corroborated by any significant relationship between consolidation improvement and sleep parameters and indices on post-training night, whereas a significant relationship between REM density in the first half of the night and next-day improvement was observed in normal subjects. As REM density has been suggested to provide a sort of biological marker of learning potential (Smith et al, 2004), this relationship can be ultimately considered consistent with previous indications (Karni et al, 1994;Plihal and Born, 1999) that REM sleep on post-training night plays an important, albeit not exclusive, role (Nissen et al, 2006;Peters et al, 2007) in the consolidation of procedural skills.…”

Rapid eye movements during sleep in mice: High trait-like stability qualifies rapid eye movement density for characterization of phenotypic variation in sleep patterns of rodents

“…In humans REM density is an important parameter that has been associated with sleep satiety [37], learning and memory [46-48] and psychiatric disorders [52]. Importantly, increased REM density has been proposed to be an endophenotype for depression [54,55] and is sensitive to treatment with antidepressants.…”

“…In animals these PGO waves have important functions in brain development and plasticity [45]. In humans increased REM density has been found after learning tasks [46-48] and, interestingly, donezepil, an acetylcholinesterase inhibitor that is used in the treatment of Alzheimer's disease, was found to increase REM density and memory in healthy subjects [49-51]. …”

Sleep in children improves memory performance on declarative but not procedural tasks

“…Declarative memories benefit particularly from slow wave sleep (SWS), whereas procedural memories benefit particularly from REM sleep (Plihal and Born 1997;Peigneux et al 2004;Marshall and Born 2007), aside from distinct contributions of non-REM sleep stage 2 to memory consolidation (Gais et al 2002;Fogel and Smith 2006;Peters et al 2007). Childhood, compared with adulthood, is characterized not only by distinctly greater amounts of sleep and SWS (Anders et al 1995;Ohayon et al 2004) but also by a tremendous extent of brain and behavioral plasticity, determining the child's capability to rapidly acquire huge amounts of facts and to effectively shape skills in response to environmental challenges (Li et al 2006;Brehmer et al 2007).…”